Environmental Enrichment. for Nonhuman Primates. Resource Guide (Updated October 2009) AWIC Resource Series No. 32. Photo courtesy Photos8.

Transcription

1 United States Department of Agriculture Environmental Enrichment Agricultural Research Service for Nonhuman Primates National Agricultural Library Resource Guide Animal Welfare Information Center 2006 (Updated October 2009) Photo courtesy Photos8.com AWIC Resource Series No. 32

2

3 United States Department of Agriculture Agricultural Research Service National Agricultural Library Animal Welfare Information Center Environmental Enrichment for Nonhuman Primates Resource Guide AWIC Resource Series No (Updated October 2009) Compiled by: Kristina M. Adams, M.S. Animal Welfare Information Center National Agricultural Library U.S. Department of Agriculture Beltsville, Maryland Web site: Available online:

4 National Agricultural Library Cataloging Record Adams, Kristina M. Environmental Enrichment for Nonhuman Primates Resource Guide [electronic resource] AWIC Resource Series No. 32, Updated 1. Environmental enrichment (Animal culture) -- Bibliography. 2. Primates -- Environmental Enrichment -- Bibliography. I. Animal Welfare Information Center (U.S.) II. Title. ahv4701.a94 no. 32, Updated Disclaimers The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or a part of an individual s income is derived from any public assistance program. (Not all prohibited bases apply to all programs.) Persons with disabilities who require alternative means for communication of program information (Braille, large print, audiotape, etc.) should contact USDA s TARGET Center at (202) (voice and TDD). To file a complaint of discrimination write to USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, D.C or call (800) (voice) or (202) (TDD). USDA is an equal opportunity provider and employer. The use of trade, firm, or corporation names in this publication (or page) is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable. Materials appearing in this publication do not necessarily represent positions or policies of the U.S. Department of Agriculture or any agencies thereof.

5 Table of Contents About this Document Introduction U.S. Government Agency Information U.S. Laws, Regulations and Guidelines for Environmental Enhancement of Nonhuman Primates Animal Behavior Research Findings Facilitate Comprehensive Captive Animal Care: The Birth of Behavioral Management by J.L. Weed and P.L. O Neill-Wagner, National Institutes of Health iii v vii ix xiv Bibliography General Environmental Enrichment 1 General Primate Enrichment 13 Abnormal Behavior 27 Great Apes and Gibbons 47 Macaques 65 Old World Monkeys 81 Marmosets and Tamarins 87 New World Monkeys 97 Lemurs, Lorises and Tarsiers 103 Training 109 Books and Conference Proceedings 119 Web Site Information Online Resources 123 Organizations and Professional Societies 127 U.S. National Primate Centers 131 Additional Primate Centers and Animal Colonies 133 Products and Suppliers 135 Discussion Groups 139 USDA Final Report and Draft Policy Final Report on Environmental Enhancement to Promote the Psychological Well-being of Nonhuman Primates 141 USDA Draft Policy on Environmental Enhancement for Nonhuman Primates 243 Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) i

6 ii

7 About this Document This publication updates the Environmental Enrichment for Nonhuman Primates Resource Guide, AWIC Resource Series No June This document includes the draft policy published in the Federal Register on July 15, 1999 by the United States Department of Agriculture, Animal and Plant Health Inspection Service, Animal Care and the Final Report on Environment Enhancement to Promote the Psychological Well-being of Nonhuman Primates that was drafted by a committee of experts from areas of research, teaching, regulation, and exhibition and led to the draft policy. Relevant sections of United States Animal Welfare Act and regulations are also included as well as parts of the Guide for the Care and Use of Laboratory Animals (NRC, 1996; The bibliographic chapters are divided into subject areas that cover the concept of environmental enrichment, enrichment for nonhuman primates overall, abnormal behavior exhibited by nonhuman primates, great apes and gibbons, macaques, old world monkeys other than macaques, marmosets and tamarins, other new world monkeys, lemurs, lorises, and tarsiers, animal training as an enrichment strategy, and books and proceedings from conferences focused on environmental enrichment or nonhuman primate management. Citations included in these chapters were published between 1999 and October 2009 and selected from searches conducted using a variety of agricultural, medical and life science databases. In each chapter, the citations are arranged alphabetically according to the last name of the primary author. Each citation in the bibliography contains descriptor terms, an abstract when available, and the NAL call number if the particular source is available at the National Agricultural Library (NAL). Information on how to request materials that are included in the collection of the National Agricultural Library (NAL) may be found on the Request Library Materials page ( Please read carefully as there are certain restrictions on media and document types. All patrons are encouraged to explore local library resources first before contacting the National Agricultural Library. The Web site resources are divided into 6 sections: resources on environmental enrichment, for all species and nonhuman primates,organizations and professional societies whose members may be involved in nonhuman primate management or research, United States National Primate Centers, funded by grants through the National Institutes of Health (NIH), National Center for Research Resources (NCRR), Division of Comparative Medicine (DCM), additional university primate centers and animal colonies located in the United States and associated territories, environmental enrichment products and supplier information, and Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) iii

8 discussion groups on nonhuman primates and enrichment. Readers are cautioned as to the dynamic nature of the internet and the fact that web addresses and content are subject to change. All sites are current as of October Acknowledgements The editor would like to thank Dr. Jodie Kulpa-Eddy of USDA, APHIS, Animal Care for her comments and editing of the introductory material for this document. Thank you to Jean Larson of the USDA Animal Welfare Information Center for her guidance on document lay-out and thorough editing of the entire document. Finally, special thanks to Sandra Ball of the Animal Welfare Information Center for the Web publishing of this document. iv About this Document

9 Introduction In 1985, the Animal Welfare Act (AWA) was amended to include, among other things, providing for the psychological well-being of nonhuman primates. In time this concept became synonymous with the terms environmental enrichment or environmental enhancement. The Congressional delegates responsible for the new amendments intended to allow for more exercise, play, and compatible social interactions for captive nonhuman primates. In 1989, the United States Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS) responded to the new AWA amendments by drafting regulations based on the advice received from a group of 10 primate experts. These proposed regulations contained requirements for social housing, inanimate enrichment items, and exercise for nonhuman primates. APHIS eventually amended the regulations with more general language after receiving public comments on the proposed standards. The regulations became a final rule in 1991 and still exist today (9 CFR Sec. 3.81). (For more information on the history and intent of the 1985 amendments, see Kulpa-Eddy et al., 2005.) After five years of enforcing the regulations on environmental enrichment for nonhuman primates, APHIS surveyed their Animal Care (AC) inspectors about the implementation of enrichment plans at research facilities, exhibitors, and dealers. The consensus among AC inspectors was that most facilities did not understand how to develop an adequate environmental enrichment plan that would promote the well-being of nonhuman primates. In response to this concern, additional clarification was set forth in the Final Report on Environment Enhancement to Promote the Psychological Well-being of Nonhuman Primates which was included in a draft policy and issued for public comment on July 15, Ultimately, the policy was not implemented. However, the draft policy and Final Report did provide a great deal of science-based information for facilities housing nonhuman primates and many began implementing aspects identified under five general elements (social grouping, social needs of infants, structure and substrate, foraging opportunities, and manipulanda). Both the draft policy from the Federal Register and the Final Report on Environment Enhancement to Promote the Psychological Well-being of Nonhuman Primates are included in this information resource. Environmental enrichment is defined by the Library of Congress as enhancing the environment of confined animals in order to encourage natural behaviors and improve their quality of life (Kreger, 1999). An effective environmental enrichment program enhances species-appropriate behaviors and activities, increases behavioral choices, and encourages appropriate responses to environmental challenges. Environmental enrichment for nonhuman primates can include provision of novel objects, increased foraging opportunities, and opportunities for social interaction. After the 1985 AWA amendments, many facilities initially approached environmental enrichment as simply giving the animals toys. However, in response to published research and input from specialists, including the writers of the USDA draft policy, many facilities housing nonhuman primates now regard their enrichment plans as part of a larger behavioral health and management program. Weed and O Neill- Wagner (2006) discuss the evolution of behavioral management programs in zoos and laboratory research environments starting on page xvii of this document. The creation of a successful behavioral management program and subsequent environmental enrichment plan is based on an understanding of the natural history of each particular species. Facilities that maintain nonhuman primates in captivity develop enrichment plans by taking into account species-appropriate behavior, Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) v

10 individual animals medical and behavioral histories, and the current limitations of the setting. The safety of the animals and personnel should always be considered. In the United States, USDA, APHIS, AC is responsible for enforcement of the AWA. AC implements the standards for humane care set forth in the AWA and regulations and achieves compliance through inspections of regulated facilities, educational programming, and cooperative efforts with other agencies and organizations. For laboratory animal care, the National Institutes of Health (NIH), Office of Laboratory Animal Welfare (OLAW) enforces the Public Health Service (PHS) Policy on Humane Care and Use of Laboratory Animals for researchers receiving federal funding from PHS. The contact information for both agencies is provided in the following section. References Kreger, M. (1999). Environmental Enrichment for Nonhuman Primates Resource Guide. USDA, Animal Welfare Information Center: Beltsville, Maryland, USA, 115 p. Kulpa-Eddy, J.A., S. Taylor, and K. Adams (2005). USDA Perspective on Environmental Enrichment for Animals. ILAR Journal 46(2): Weed, J.L. and P.L. O Neill-Wagner (2006). Animal behavior research findings facilitate comprehensive captive animal care: The birth of behavioral management. In: Environmental Enrichment for Nonhuman Primates Resource Guide, AWIC Resource Series No. 32, Updated USDA, Animal Welfare Information Center: Beltsville, Maryland, USA, 262 p. vi Introduction

11 U.S. Government Agency Information U.S. Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS), Office of Animal Care (AC) APHIS/AC enforces the Animal Welfare Act and develops animal care regulations for exhibitors, researchers, and animal dealers. APHIS/AC answers questions regarding the regulations including those about the psychological well-being of nonhuman primates. The staff also refers patrons to regional offices where they can communicate directly with Animal Care inspectors and veterinary medical officers. Contact Information: 4700 River Road Unit 84 Riverdale, Maryland USA Tel: (301) ; Fax: (301) Web: Department of Health and Human Services (DHHS), National Institutes of Health (NIH), Office of Laboratory Animal Welfare (OLAW) Located at the NIH, Office of Extramural Research, OLAW enforces the PHS Policy on Humane Care and Use of Laboratory Animals for researchers who receive Public Health Service funding. It produces conferences and workshops relating to responsible animal care and use in biomedical research. OLAW can provide guidance on the development of plans to enhance psychological well-being of nonhuman primates. The PHS Policy requires adherence to the Animal Welfare Act regulations and the Guide for the Care and Use of Laboratory Animals. Contact Information: National Institutes of Health, Office of Extramural Research OLAW, Division of Animal Welfare 6100 Executive Blvd., Suite B01 Rockville, Maryland USA Tel: (301) ; Fax: (301) Web site: Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) vii

12 viii

13 U.S. Laws, Regulations and Guidelines for Environmental Enrichment of Nonhuman Primates In the 1985 amendments to the Animal Welfare Act (Improved Standards for Laboratory Animals Act), Congress included mention of psychological well -being for nonhuman primates. Included below are the text from the Animal Welfare Act and the final version of the regulations as they appear in the Code of Federal Regulations. In addition to the Animal Welfare Act, those who receive funding from the Public Health Service or are accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC) must also comply with the Guide for the Care and Use of Laboratory Animals, which is based on a performance standards approach. The 1996 Guide is intended to assist institutions in caring for and using animals in ways judged to be scientifically, technically, and humanely appropriate. The Guide contains standards related to environmental enrichment in the section Animal Environment, Housing and Management and are included below. Animal Welfare Act as amended 7 U.S.C Standards and certification process for humane handling, care, treatment, and transportation of animals (a)(1) The Secretary shall promulgate standards to govern the humane handling, care, treatment, and transportation of animals by dealers, research facilities, and exhibitors. (2) The standards described in paragraph (1) shall include minimum requirements-- (B) for exercise of dogs, as determined by an attending veterinarian in accordance with the general standards promulgated by the Secretary, and for a physical environment adequate to promote the psychological well-being of primates. Title 9, Code of Federal Regulations, Subchapter A Animal Welfare Part 3 Standards, Subpart D Specifications for the Humane Handling, Care, Treatment, and Transportation of Nonhuman Primates, Section 3.81 Sec Environment enhancement to promote psychological well-being. Dealers, exhibitors, and research facilities must develop, document, and follow an appropriate plan for environment enhancement adequate to promote the psychological well-being of nonhuman primates. The plan must be in accordance with the currently accepted professional standards as cited in appropriate professional journals or reference guides, and as directed by the attending veterinarian. This plan must be made available to APHIS upon request, and, in the case of research facilities, to officials of any pertinent funding agency. The plan, at a minimum, must address each of the following: Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) ix

14 (a) Social grouping. The environment enhancement plan must include specific provisions to address the social needs of nonhuman primates of species known to exist in social groups in nature. Such specific provisions must be in accordance with currently accepted professional standards, as cited in appropriate professional journals or reference guides, and as directed by the attending veterinarian. The plan may provide for the following exceptions: (1) If a nonhuman primate exhibits vicious or overly aggressive behavior, or is debilitated as a result of age or other conditions (e.g., arthritis), it should be housed separately; (2) Nonhuman primates that have or are suspected of having a contagious disease must be isolated from healthy animals in the colony as directed by the attending veterinarian. When an entire group or room of nonhuman primates is known to have or believed to be exposed to an infectious agent, the group may be kept intact during the process of diagnosis, treatment, and control. (3) Nonhuman primates may not be housed with other species of primates or animals unless they are compatible, do not prevent access to food, water, or shelter by individual animals. and are not known to be hazardous to the health and well-being of each other. Compatibility of nonhuman primates must be determined in accordance with generally accepted professional practices and actual observations, as directed by the attending veterinarian, to ensure that the nonhuman primates are in fact compatible. Individually housed nonhuman primates must be able to see and hear nonhuman primates of their own or compatible species unless the attending veterinarian determines that it would endanger their health, safety, or well-being. (b) Environmental enrichment. The physical environment in the primary enclosures must be enriched by providing means of expressing noninjurious species-typical activities. Species differences should be considered when determining the type or methods of enrichment. Examples of environmental enrichments include providing perches, swings, mirrors, and other increased cage complexities; providing objects to manipulate; varied food items; using foraging or task-oriented feeding methods; and providing interaction with the care giver or other familiar and knowledgeable person consistent with personnel safety precautions. (c) Special considerations. Certain nonhuman primates must be provided special attention regarding enhancement of their environment, based on the needs of the individual species and in accordance with the instructions of the attending veterinarian. Nonhuman primates requiring special attention are the following: (1) Infants and young juveniles; (2) Those that show signs of being in psychological distress through behavior or appearance; (3) Those used in research for which the Committee-approved protocol requires restricted activity; (4) Individually housed nonhuman primates that are unable to see and hear nonhuman primates of their own or compatible species; and (5) Great apes weighing over 110 lbs. (50 kg). Dealers, exhibitors, and research facilities must include in the environment enhancement plan special provisions for great apes weighing over 110 lbs. (50 kg), including additional opportunities to express species-typical behavior. (d) Restraint devices. Nonhuman primates must not be maintained in restraint devices unless required for health reasons as determined by the attending veterinarian or by a research proposal approved by the Committee at research facilities. Maintenance under such restraint must be for the shortest period possible. In instances where long-term (more than 12 hours) restraint is required, the nonhuman primate must be provided the opportunity daily for unrestrained activity for at least one continuous hour during the period of restraint, unless continuous restraint is required by the research proposal approved by the Committee at research facilities. (e) Exemptions. (1) The attending veterinarian may exempt an individual nonhuman primate from participation in the environment enhancement plan because of its health or condition, or in consideration of its well-being. The basis of the exemption must be recorded by the attending veterinarian for each exempted nonhuman primate. Unless the basis for the x U.S. Laws, Guidelines and Regulations

15 exemption is a permanent condition, the exemption must be reviewed at least every 30 days by the attending veterinarian. (2) For a research facility, the Committee may exempt an individual nonhuman primate from participation in some or all of the otherwise required environment enhancement plans for scientific reasons set forth in the research proposal. The basis of the exemption shall be documented in the approved proposal and must be reviewed at appropriate intervals as determined by the Committee, but not less than annually. (3) Records of any exemptions must be maintained by the dealer, exhibitor, or research facility and must be made available to USDA officials or officials of any pertinent funding Federal agency upon request. (Approved by the Office of Management and Budget under control number ) Guide for the Care and Use of Laboratory Animals National Research Council (1996). Guide for the Care and Use of Laboratory Animals. National Academy Press: Washington, D.C., 127p. Animal Environment, Housing and Management Proper housing and management of animal facilities are essential to animal well-being, to the quality of research data and teaching or testing programs in which animals are used, and to the health and safety of personnel. A good management program provides the environment, housing, and care that permit animals to grow, mature, reproduce, and maintain good health; provides for their well-being; and minimizes variations that can affect research results. Specific operating practices depend on many factors that are peculiar to individual institutions and situations. Well-trained and motivated personnel can often ensure high-quality animal care, even in institutions with less than optimal physical plants or equipment. Many factors should be considered in planning for adequate and appropriate physical and social environment, housing, space, and management. These include The species, strain, and breed of the animal and individual characteristics, such as sex, age, size, behavior, experiences, and health. The ability of the animals to form social groups with conspecifics through sight, smell, and possibly contact, whether the animals are maintained singly or in groups. The design and construction of housing. The availability or suitability of enrichments. The project goals and experimental design (e.g., production, breeding, research, testing, and teaching). The intensity of animal manipulation and invasiveness of the procedures conducted. The presence of hazardous or disease-causing materials. The duration of the holding period. Animals should be housed with a goal of maximizing species-specific behaviors and minimizing stress-induced behaviors. For social species, this normally requires housing in compatible pairs or groups. A strategy for achieving desired housing should be developed by animal-care personnel with review and approval by the IACUC. Decisions by the IACUC in consultation with the investigator and veterinarian, should be aimed at achieving high standards for professional and husbandry practices Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) xi

16 considered appropriate for the health and well-being of the species and consistent with the research objectives. After the decision-making process, objective assessments should be made to substantiate the adequacy of animal environment, husbandry, and management. The environment in which animals are maintained should be appropriate to the species, its life history, and its intended use. For some species, it might be appropriate to approximate the natural environment for breeding and maintenance. (Chapter 2, pages 21-22) Naturalistic Environments Areas like pastures and islands afford opportunities to provide a suitable environment for maintaining or producing animals and for some types of research. Their use results in the loss of some control over nutrition, health care and surveillance, and pedigree management. These limitations should be balanced against the benefits of having the animals live in more natural conditions. Animals should be added to, removed from, and returned to social groups in this setting with appropriate consideration of the effects on the individual animals and on the group. Adequate supplies of food, fresh water, and natural or constructed shelter should be ensured. (Chapter 2, page 25) Structural Environment The structural environment consists of components of the primary enclosure-cage furniture, equipment for environmental enrichment, objects for manipulation by the animals, and cage complexities. Depending on the animal species and use, the structural environment should include resting boards, shelves or perches, toys, foraging devices, nesting materials, tunnels, swings, or other objects that increase opportunities for the expression of species-typical postures and activities and enhance the animals well-being. Much has been learned in recent years about the natural history and environmental needs of many animals, but continuing research into those environments that enhance the well-being of research animals is encouraged. Selected publications that describe enrichment strategies for common laboratory animal species are listed in Appendix A and in bibliographies prepared by the Animal Welfare Information Center (AWIC 1992; NRC In press). Social Environment Consideration should be given to an animal s social needs. The social environment usually involves physical contact and communication among members of the same species (conspecifics), although it can include noncontact communication among individuals through visual, auditory, and olfactory signals. When it is appropriate and compatible with the protocol, social animals should be housed in physical contact with conspecifics. For example, grouping of social primates or canids is often beneficial to them if groups comprise compatible individuals. Appropriate social interactions among conspecifics are essential for normal development in many species. A social companion might buffer the effects of a stressful situation (Gust and others 1994), reduce behavioral abnormality (Reinhardt and others 1988, 1989), increase opportunities for exercise (Whary and others 1993), and expand species-typical behavior and cognitive stimulation. Such factors as population density, ability to disperse, initial familiarity among animals, and social rank should be evaluated when animals are being grouped (Borer and others 1988; Diamond and others 1987; Drickamer 1977; Harvey and Chevins 1987; Ortiz and others 1985; Vandenbergh 1986, 1989). In selecting a suitable social environment, attention should be given to whether the animals are naturally territorial or communal and whether they should be housed singly, in pairs, or in groups. An understanding of species-typical natural social behavior will facilitate successful social housing. xii U.S. Laws, Guidelines and Regulations

17 However, not all members of a social species can or should be maintained socially; experimental, health, and behavioral reasons might preclude a successful outcome of this kind of housing. Social housing can increase the likelihood of animal wounds due to fighting (Bayne and others 1995), increase susceptibility to such metabolic disorders as atherosclerosis (Kaplan and others 1982), and alter behavior and physiologic functions (Bernstein 1964; Bernstein and others 1974a,b). In addition, differences between sexes in compatibility have been observed in various species (Crockett and others 1994; Grant and Macintosh 1963; Vandenbergh 1971; vom Saal 1984). These risks of social housing are greatly reduced if the animals are socially compatible and the social unit is stable. It is desirable that social animals be housed in groups; however, when they must be housed alone, other forms of enrichment should be provided to compensate for the absence of other animals, such as safe and positive interaction with the care staff and enrichment of the structural environment. (Chapter 2, pages 36-38) Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) xiii

18 xiv U.S. Laws, Guidelines and Regulations

19 Animal Behavior Research Findings Facilitate Comprehensive Captive Animal Care: The Birth of Behavioral Management J.L. Weed, Division of Veterinary Resources, Office of Research Services, National Institutes of Health, DHHS. P. L. O Neill-Wagner, Laboratory of Comparative Ethology, NIH Animal Center, Poolesville, Maryland, NICHD, PHS, DHHS. Short title: Behavioral management and captive care Corresponding author: J. L. Weed 9000 Rockville Pike Bldg 14G, MSC 5590 Bethesda, MD weedj@mail.nih.gov During the past several decades there has been an explosive increase in animal behavior research in captive and wild animal populations. This growing body of scientific investigation expands the understanding of basic principles xiv Behavioral Management and Captive Care

20 During the past several decades there has been an explosive increase in animal behavior research in captive and wild animal populations. This growing body of scientific investigation expands the understanding of basic principles underlying animal behavior relative to biology, psychology, ecology, and natural history. As scientific research reveals increasing detail about the mechanisms influencing and driving animal behavior, the ability to appropriately manage and enhance the captive animal experience is opened to more possibilities and options including the area of animal well-being. In fact, this expanding informational resource is being applied today by a new breed of experts, Animal Behavior Managers, found working worldwide in facilities such as zoos, animal breeding colonies, and biomedical research institutions. What prompted this shift from scientific discovery to applied principles of animal management? Some would consider the passage of welfare legislation (AWA, 1985) to be a defining moment for the regulatory acceptance and application of animal behavior research findings. While this legislation formally codified the idea of environmental enhancement and introduced the phrase psychological well-being, the concept had already been described in the 1972 and 1985 editions of The Guide for the Care and Use of Laboratory Animals (The Guide) and was likely the influence for later legislation. The Guide, published by the National Research Council through the Institute for Laboratory Animal Resources and the National Institutes of Health, is intended to assist scientific institutes in providing professionally appropriate care for laboratory animals. Proper management is defined in the 1972 Guide as any system of housing and care that permits animals to grow, mature, reproduce, or behave normally, and to be maintained in physical comfort and good health. Elsewhere in the 1972 edition, the term psychological well-being was utilized relative to physical activity and exercise. Revisions to the 1985 Guide include the recommendation that consideration be given to enriching the environment. The term Behavioral Management also first appeared in the same edition and describes various ways to promote well being by providing social opportunities, structural complexities, and stimulating activities for captive animals. These regulations and guidelines responded to behavior goals for achieving psychological well-being using environmental enhancements in addition to the traditional clinical, husbandry, and design aspects of captive animal management. From Environment Based to Behavior Based Terminology Markowitz (1974; 1978) proposed a term Behavioral Engineering to describe changes in zoo collection management to expand the range and expression of natural behavior of the animals and thereby improve the animals well-being. These changes included implementing naturalistic feeding, problem-solving, and locomotor challenges for the animals. As a result of Markowitz s innovations, animals began to engage in more species typical behavior. This allowed zoo animal managers to improve the visual, auditory, and learning experience of the zoo visitors, while stimulating and enriching the captive animals. Although it appeared to be a win-win situation his concept initially met with limited acceptance from the zoological community, likely due to the terminology. Zoo professionals were concerned that Behavioral Engineering terminology meant engineering the animal s behavior rather than engineering environments that improved the animal s well being (Markowitz, 1982; Markowitz, personal communication, 2006). Similarly, the term Environmental Enrichment has experienced difficulties since its inception. Newberry (1995) describes some of the problems associated with this term. The difficulty with the EE terminology is due to a limited number of scientifically guided assessments of enrichment techniques or procedures and hard evidence regarding effectiveness in actual use. The EE catch phrase came to include any implementation of changes in the captive animal s space regardless of the overall impact. Even though enrichment plans evolved out of the Animal Welfare Regulation mandate to enhance the environment those plans dedicated solely to enriching the animal s physical environment often fell short of desired behavioral outcomes due to individual animal social and housing needs, rearing history, biology, genetic makeup, developmental life stage, and experimental stressors. Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) xv

21 A number of approaches focused more on structured activities such as individual animal training, socialization, and dietary diversity, to meet the needs of individual animals and researchers. Plans have been referred to as Behavioral Performance Plans (Swaisgood, & Sheperdson, 2005), Refined Husbandry and Management Plans, (Rice, 1994), Clinical Ethology Plans (Ladewig, 2005), Wildlife Management Plans for the Laboratory (Bayne, 1995), Interdisciplinary Approaches (Lund et al., 2006), Cooperative Approaches (Reinhardt & Cowley, 1990; Vertein & Reinhardt, 1989), and Time Management Plans (Schwammer, 1997), just to name a few. Approaches differed in their attention toward individual animal needs. Treatment and prevention of individual behavior problems varied widely, as did performance training of animals relative to implementation of specific research protocols. While some environments allowed for expression of species normative behavior in captivity, others did not. Variation in terminology and focus very likely corresponded to variation in behavioral results. Animal responses to routine and standardized enrichment techniques have been wide-ranging, at times unanticipated, and even counter intuitive to popular belief (cf. Line et al., 1990; Markowitz & Timmel, 2005; Morgan et al., 1998). Observing these diverse responses offered a much needed opportunity for reevaluating the systematic approach required to achieve well-being. Reviews by Bloomsmith & Else, 2005; Kulpa-Eddy et al., 2005; and Lutz & Novak, 2005, provide a historical perspective on the evolution of enrichment programs for animals with particular attention to programs for nonhuman primates. This lack of standardized enrichment implementation and diversity of outcomes most likely led to the widespread use of the more popular Behavioral Management terminology. From Technically Based to Scientifically Based Enrichment It is also likely that transitioning from the most prevalent term Environmental Enrichment to the less familiar Behavioral Management required a common purpose to gain acceptance. Use of the term Behavioral Management suggests a broader program scope regardless of whether it is implicitly or explicitly stated in any formal documentation (Rice et al., 2002). There also seems to be a general consensus from the literature that captive animal welfare programs are gradually evolving from technically based to scientifically based programs. This is a sensible transition since vast resources of scientific literature and clinically logged data continue to develop a strong foundation that allows for more comprehensive animal husbandry and clinical care programs. These advancements have taken generic environmentally based enrichment plans to a more scientific individualized animal enrichment technology based upon known relationships between the animal s environment, from birth to maturity, and its overall behavior profile. Although scientifically based assessments of enrichment programs are in their infancy (Baker et al., 2006; Bloomsmith & Else, 2005; Crockett, 1998), current behavioral management plans at zoos and in primate laboratories have successfully advanced to a point where the behavioral and clinical needs of animals in socially and physically stimulating environments are currently an integral component of the overall animal program (Bloomsmith & Else, 2005; Maple & Archibald, 1991). Collaborative programs between clinical and behavioral specialists at these facilities are becoming the standard rather than the exception. Baker et al. (2006) surveyed several laboratory and university facilities which house nonhuman primates. The focus of the survey was enrichment and behavioral management. They found that nearly half of all enrichment program managers working at primate facilities had formal training in behavior methods. The day-to-day behavioral management of the animals is increasingly tasked to individuals trained specifically in animal behavior and assessment techniques. The impetus for this change may be due in part to the concerted efforts of a few individuals who began their careers working in the zoo community and in some cases managing primate research facilities. Gail Laule and Tim Desmond were among the first to formally document methods for enhancing the captive experience for zoo and laboratory animals (Desmond, 1994; Laule, 1993). One individual in particular, Dr. Michale Keeling, formerly xvi Behavioral Management and Captive Care

22 at the M.D. Anderson Cancer Center in Texas, demonstrated great foresight by adopting these behavioral management techniques to the laboratory (Keeling et al., 1991). Dr. Keeling was a program director who realized the benefits of hiring individuals with behavioral backgrounds to work in the primate laboratory at Bastrop, Texas. Keeling and his colleagues (Keeling et al., 1991) proposed a strong bias for action regarding the management of primates and enrichment programs in laboratories. Many of those management tenets for working with nonhuman primates have become commonplace in the general laboratory and zoological community (Bloomsmith et al., 1991; Schapiro, 2000; Schapiro et al., 2003; Schapiro et al., 1994; Schapiro et al., 2005; Whittaker et al., 2001; NRC, 1998). It is clear that the major focus of current environmental enhancement programs is more than just providing supplemental toys for animals to manipulate. This is true regardless of whether animals are housed in a research laboratory or zoological collection. The concept of behavioral management addresses questions about animal behavior as a critical and integral component of the overall health and well-being of these animals. Benefits from the efforts of dedicated animal behavior specialists working at all levels of laboratory and zoo collection management are being experienced by the animals as well as veterinarians, principal investigators, animal care staff, business office managers and the general public. Programs will continue to evolve and address well-being as more data are generated allowing improved captive animal management. The challenge for the future is to continue finding support for scientifically updating the principles and procedures of behavioral management. Markowitz and Timmel (2005) point out that there is continued reluctance from funding agencies to support needed basic research into issues relative to facility design, husbandry techniques or behavioral methods which potentially enhance animal well-being. Continued support from individuals responsible for laboratory and zoological review, accreditation, and oversight is critical to move these programs forward. This is especially true if the principles advocated by practitioners of behavioral management are to ultimately gain acceptance as the new standards of animal care. Acknowledgments J. L. Weed is supported by the Intramural Research Program of the NIH, Division of Veterinary Resources, Office of Research Services. Peggy O Neill-Wagner is supported by the Intramural Research Program of the National Institute of Child Health and Human Development, Laboratory of Comparative Ethology. Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) xvii

23 References AWA [Animal Welfare Act] Food security act of 1985, Public Law Washington DC: GPO. Baker, K.C., Weed, J.L., Crockett, C.M., Bloomsmith, M.A Survey of environmental enhancement programs for laboratory primates. Am J Primatol. In press. Bayne, K.A.L Wildlife management in the laboratory: Nonhuman primates. In: Wildlife Mammals as Research Models: In the Laboratory and the Field. Proceedings of a seminar sponsored by Scientists Center for Animal Welfare at American Veterinary medical Association meeting, July 12, K. Bayne and M. Kreger, Eds Bloomsmith, M.A., Brent, L.Y., Schapiro, S.J Guidelines for developing and managing and environmental enrichment program for nonhuman primates. Laboratory Animal Science, 41: Bloomsmith, M.A. & Else, J.G Behavioral management of chimpanzees in biomedical research facilities: the state of the science. ILAR J. 46: Crockett, C.M Psychological well-being of captive nonhuman primates: lessons from laboratory studies. In: Sheperdson, D., Mellen, J., and Hutchins, M. eds. Second Nature. Smithsonian Institution Press. Washington, DC. pp Desmond, T Behavioral management - an integrative approach to animal care. Proceedings of the American Association of Zoological Parks and Aquariums Annual Conference. Pp Keeling, M.E., Alford, P.L., Bloomsmith, M.A Decision analysis for developing programs of psychological well-being: a bias-for-action approach. Pg In: Through the looking glass. Issues of psychological well-being in captive nonhuman primates. M.A. Novak, A.J. Petto, Eds. American Psychological Association, Washington, DC Kulpa-Eddy, J.A., Taylor, S., Adams, K.M USDA perspective on environmental enrichment for animals. ILAR J. 46: Ladewig, J Of mice and men: Improved welfare through clinical ethology. Applied Animal Behaviour Science. 92: Laule, G The use of behavioral management techniques to reduce or eliminate abnormal behavior. AWIC newsletter, 4: Line, S.W., Morgan, K.N., Markowitz, H., Strong, S Increased cage size does not alter heart rate or behavior in female rhesus monkeys. Am J Primatol 20: Lund, V., Coleman. G., Gunnarson, S., Appleby, M.C., Karkinen, K Animal Welfare Science-Working at the interface between the natural and social sciences. Applied Animal Behaviour Science, 97: Maple, T. L. & Archibald, E.F Zoo man. Longstreet Press:Atlanta. Markowitz, H Analysis and control of behavior in the zoo. In: Research in zoos and aquariums. Washington: National Academy of Sciences. Pp Markowitz, H Engineering environments for behavioral opportunities in the zoo. Behavior Analyst, 1: Markowitz, H Behavioral enrichment in the zoo. Van Nostrand Reinhold: New York. xviii Behavioral Management and Captive Care

24 Markowitz, H. & Timmel, G.B Animal well-being and research outcomes. In: Mental health and well-being in animals. F.D. Macmillan (ed). Blackwell. Ames, Iowa. Pp Morgan, K.N., Line, S.W., Markowitz, H Zoos, enrichment, and the skeptical observer. In: Sheperdson, D., Mellen, J., and Hutchins, M. eds. Second Nature. Smithsonian Press. Washington, DC. Pp NRC [National Research Council] Psychological well-being of nonhuman primates. Washington DC: National Academy Press. Newberry, R.C Environmental enrichment: Increasing the biological relevance of captive environments. Appl Anim Behav Sci 44: Reinhardt, V., Cowley, D Training Stumptailed monkeys (Macaca arctoides) to cooperate during in-homecage treatment. Laboratory Primate Newsletter 29:9-10. Rice, J.M Zoo husbandry and research: an integrated approach. Humane Innovations and Alternatives, 8: Rice, T.R., Walden, S., Laule, G.E., Heidbrink, G.A Behavioral management: It s everyone s job. Cont Topics, 41, Schapiro, S.J A few new developments in primate housing and husbandry. Scand J Lab Anim Sci, 27, Schapiro, S.J., Bloomsmith, M.A., Laule, G.E Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science, 6: Schapiro, S.J., Lee-Parritz, D.E., Taylor, L.L., Watson, L., Bloomsmith, M.A., Petto, A Behavioral management of specific pathogen-free rhesus macaques: group formation, reproduction, and parental competence. Laboratory Animal Science, 44, Schapiro, S.J., Perlman, J.E., Thiele, E., Lambeth, S Training nonhuman primates to perform behaviors useful in biomedical research. Lab Animal, 34: Schwammer, H.M Time management for zoo animals: Behavioral problems in captivity and their management. In: Proceedings of the 2nd International Conference On Environmental Enrichment, August 195, Copenhagen B. Holst, ed. Copenhagen Zoo, Frederiksberg, pp Swaisgood, R.R., Sheperdson, D.J Scientific approaches to enrichment and stereotypies in zoo animals: What s been done and where should we go next? Zoo Biology, 24: U.S. Public Health Service Guide for the Care and Use of Laboratory Animals. NIH Bethesda, MD.: National Institutes of Health. U.S. Public Health Service Guide for the Care and Use of Laboratory Animals. NIH Bethesda, MD.: National Institutes of Health. Vertein, R., Reinhardt, V Training female rhesus monkeys to cooperate during in-homecage venipuncture. Laboratory primate Newsletter, 28:1-3. Whittaker, M., Laule, G., Perlman, J., Schapiro, S., Keeling, M Behavioral management approach to caring for great apes. The Apes: Challenges for the 21st Century. Conference proceedings. May 10-13, Brookfield, Illinois. Pp Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) xix

25 General Environmental Enrichment Anonymous (2004). Looking after animals kept in research laboratories. Animal Welfare Institute Quarterly 53(2): online (1-3). Online: Descriptors: colony managment, animal welfare, environmental enrichment, list-serv discussion. Anonymous (2002). Refinement and environmental enrichment database. Alternatives to Laboratory Animals 30(6): 567. ISSN: Online: NAL Call Number: Z7994.L3A5 Descriptors: introduction to electronic database, online enrichment resource, Animal Welfare Institute. Anonymous (2003). Toying with enrichment options. Lab Animal 32(10): 7. ISSN: NAL Call Number: QL55.A1L33 Descriptors: aggression, environmental enrichment, music, species differences, social interactions. Anonymous (2003). The welfare of zoo animals. Journal of the American Veterinary Medical Association 223(7): ISSN: NAL Call Number: 41.8 Am3 Descriptors: special journal supplement, animal well-being, ethics, wild animals in captivity, strategic collection planning, positive reinforcement training, environmental enrichment, stress, zoo design, animal surpluses. Notes: Meeting Information: 2002 AVMA Animal Welfare Forum, Milwaukee, Wisconsin, USA; October 11, AAZK Enrichment Committee (2004). Enrichment Notebook, 3rd Edition, AAZK, Inc.: Topeka, Kansas, USA, ISBN: X. [CD-Rom] NAL Call Number: SF A Descriptors: environmental enrichment, zoo animals, bibliography. Balcombe, J.P., N.D. Barnard, and C. Sandusky (2004). Laboratory routines cause animal stress. Contemporary Topics in Laboratory Animal Science 43(6): ISSN: NAL Call Number: SF405.5.A23 Descriptors: stress, laboratory animals, laboratory procedures, handling, blood collection, orogastric gavage, physiological parameters, distress, humane implications. Bassett, L. and H.M. Buchanan-Smith (2007). Effects of predictability on the welfare of captive animals. Applied Animal Behaviour Science 102(3-4): ISSN: Online: NAL Call Number: QL750.A6 Descriptors: predictability of stimuli, physiological response, behavioral response, animal welfare, animal husbandry, literature review. Bayne, K. (2005). Potential for unintended consequences of environmental enrichment for laboratory animals and research results. ILAR Journal 46(2): ISSN: NAL Call Number: QL55.A1I43 Abstract: Many aspects of the research animal s housing environment are controlled for quality and/or standardization. Environmental Enrichment for Nonhuman Primates, 2006 (updated 2009) 1